Modulation of Tonically Active Neurons of the Monkey Striatum by Events Carrying Different Force and Reward Information

Abstract

The role of basal ganglia in motivational processes has been under scrutiny in recent decades, with increasing evidence from clinical studies of cognitive and motivational deficits in patients with basal ganglia lesions. Tonically active neurons (TANs), the presumed striatal cholinergic interneurons, could be important actors in integrating and relaying motivational information arising from various modalities. Their multiphasic responses to rewards and to conditioned stimuli associated with reward conferred them a role in limbic processes. They are also modulated by a task's motor aspect. Recent studies suggest they are influenced by the context in which behavioral responses are expressed. To investigate the role of TANs in motor-limbic interaction processes, we recorded 169 TANs in the striatum of two monkeys performing a motivational task, in which they had to develop a variable force to receive different amounts of reward in response to visual stimuli. Our results reveal new features of TANs response properties. First, TANs usually responded either by a pause or an elevation of discharge rate to the visual cues and the reward, with few neurons combining both pause and rebound. Second, the elevations of discharge rate after the cues were most sensitive to the least valuable (high force or small reward) task conditions. Finally, the responses of TANs to the visual cues were time locked on the onset of the animal's movement. TANs' population and responses could thus play a role in signaling less attractive situations, those with either a high motor demand and/or small reward.

Dynamic Encoding of Effort and Reward throughout the Execution of Action by External Globus Pallidus Neurons in Monkeys

“…However, given its position in the circuitry, we could expect neuronal activities in this structure reflecting an integration of motivational information, such as neuronal activities showing the same trend as the acceptance level of the monkeys or postreward activities proportionally modulated by the effort produced to obtain this reward. No population of neurons specifically encoded the cost-benefit ratio of the action or the attractiveness of the cues as found in the striatum (Nougaret & Ravel, 2015). Conversely, we have shown that neurons of the associative and limbic GPe display activities in close relationship with task parameters (i.e., motor execution and/or significance of the cues) at each step of a behavior.…”

“…Neuropsychological (Bhatia & Marsden, 1994;Laplane, Widlocher, & Pillon, 1981), human imaging (Schmidt et al, 2008;Pessiglione et al, 2007), lesion (Baunez, Dias, Cador, & Amalric, 2005;Berridge & Cromwell, 1990), and pharmacological (Grabli et al, 2004) studies have shown the involvement of several BG structures in these processes. In monkeys, the reward-related activities observed in BG input structures, such as the striatum and the subthalamic nucleus (STN; Nougaret & Ravel, 2015;Lau & Glimcher, 2008;Darbaky, Baunez, Arecchi, Legallet, & Apicella, 2005;Samejima, Ueda, Doya, & Kimura, 2005;Ravel, Legallet, & Apicella, 2003;Apicella, Ljungberg, Scarnati, & Schultz, 1991;Hikosaka, Sakamoto, & Usui, 1989), as well as in output structures, such as the internal part of the globus pallidus (GPi) and the substantia nigra pars reticulata (SNr; Joshua, Adler, Rosin, Vaadia, & Bergman, 2009;Pasquereau et al, 2007), are thought to be partly supported by dopaminergic neurons' activity (Morris, Arkadir, Nevet, Vaadia, & Bergman, 2004;Satoh, Nakai, Sato, & Kimura, 2003;.…”

Nucleus Accumbens Acetylcholine Receptors Modulate Dopamine and Motivation

“…Cholinergic signaling is elevated in situations, such as satiety (Mark et al, 1992) or disadvantageous high effort or low reward conditions (Nougaret and Ravel, 2015) that discourage vigorous reward seeking. Striatal cholinergic interneurons also express receptors for insulin, a satiety and adiposity signal, and activation of these receptors increases cholinergic activity and modulates NAc dopamine signaling through a nAChR-dependent mechanism (Stouffer et al, 2015).…”

“…Striatal cholinergic interneuron activity correlates with the presentation of reward-predictive stimuli and with motivated behavior (Morris et al, 2004;Nougaret and Ravel, 2015;Ravel et al, 2003). NAc mAChRs have been implicated in instrumental activity (Ikemoto et al, 1998;Pratt and Kelley, 2004), but neither their precise contribution, nor involvement in cue-motivated behavior has been determined.…”

Striatal Cholinergic Interneurons: How to Elucidate Their Function in Health and Disease

“…In these experiments, the animal has to execute an action to obtain a reward. These studies have revealed the involvement of CINs in more complex behavioral aspects such as contextual (Apicella, 2007), temporal (Morris et al, 2004), goaldirected action (Bradfield et al, 2013), sensori-motor gating (Ding et al, 2010), movement control/modulation (Yarom and Cohen, 2011;Nougaret and Ravel, 2015;Lee et al, 2006), and action inhibition (Lee et al, 2006). Interestingly, the expression of the pause in CIN firing is largely dependent on the behavioral task paradigm (Benhamou et al, 2014).…”